Rare earth elements (REEs) are a group of elements whose concentration in numerous environmental matrices continues to increase; therefore, the use of biological methods for their removal from soil would seem to be a safe and reasonable approach. The aim of this study was to estimate the phytoextraction efficiency and distribution of light and heavy (LREEs and HREEs) rare earth elements by three herbaceous plant species: Artemisia vulgaris L., Taraxacum officinale F.H. Wigg. and Trifolium repens L., growing at a distance of 1, 10, and 25 m from the edge of a frequented road in Poland. The concentration of REEs in soil and plants was highly correlated (r > 0.9300), which indicates the high potential of the studied plant species to phytoextraction of these elements. The largest proportion of REEs was from the group of LREEs, whereas HREEs comprised only an inconsiderable portion of the REEs group. The dominant elements in the group of LREEs were Nd and Ce, while Er was dominant in the HREEs group. Differences in the amounts of these elements influenced the total concentration of LREEs, HREEs, and finally REEs and their quantities which decreased with distance from the road. According to the Friedman rank sum test, significant differences in REEs concentration, mainly between A. vulgaris L., and T. repens L. were observed for plants growing at all three distances from the road. The same relation between A. vulgaris L. and T. officinale was observed. The efficiency of LREEs and REEs phytoextraction in the whole biomass of plants growing at all distances from the road was A. vulgaris L. > T. officinale L. > T. repens L. For HREEs, the same relationship was recorded only for plants growing at the distance 1 m from the road. Bioconcentration factor(BCF)values for LREEs and HREEs were respectively higher and lower than 1 for all studied plant species regardless of the distance from the road. The studied herbaceous plant species were able to effectively phytoextract LREEs only (BCF > 1); therefore, these plants, which are commonly present near roads, could be a useful tool for removing this group of REEs from contaminated soil. . . . . Keywords Distribution Frequented road Heavy rare earth elements Herbaceous plants Light rare earth elements Phytoextraction Introduction environmental components (van Bohemen and van de Laak 2003). As a result of the ecological consequences associated Road traffic, depending on the amount of motor vehicles, can with the high emission of toxic elements from traffic to the significantly influence the contamination of particular environment, phytoextraction of elements to aboveground plant organs growing near roads has begun to attract more attention. In literature, there are descriptions of the negative influence of Responsible editor: Elena Maestri catalytic converters responsible for the emission of platinum group elements (PGE), especially platinum (Pt), palladium * Patrycja Mleczek firstname.lastname@example.org (Pd), and rhodium (Rh) directly to the environment (Schäfer and Puchelt 1998; Kalavrouziotis and Koukoulakis 2009). 1 The other pollutants emitted by vehicles are rare earth elements Department of Ecology and Environmental Protection, Poznan (REEs), present both in soil and road dust (Djingova et al. 2003; University of Life Sciences, Piątkowska 94C, 60-649 Poznań,Poland 2 Mikołajczak et al. 2017). It is possible that the amount of vehi- Department of Mathematical and Statistical Methods, Poznan cles may be correlated with REE concentration in soil, depend- University of Life Sciences, Poznań, Poland 3 ing on a variety of environmental factors, especially the natural Faculty of Chemistry, Adam Mickiewicz University in Poznań, geological composition of the soils (Figueiredo et al. 2009). Umultowska 89B, 61-614 Poznań, Poland 23696 Environ Sci Pollut Res (2018) 25:23695–23711 A great number of studies of phytoextraction of elements in already been established (Ding et al. 2005). The concentration plants have been conducted (Simon et al. 1996; Swaileh et al. of selected REEs in soil described in the studies of Ding et al. 2004; Jankowski et al. 2014) but they have usually focused on (2005), especially Ce and Nd, increased when compared to the selected plant species and some elements only. The most com- results obtained by Ichihashi et al. (1992) or Djingova et al. monly analyzed plants—also growing near roads—are grasses (2003). It is worth underlining that increasing REEs concentra- (Jankowski et al. 2015) or herbaceous plant species such as Inula tion within the next few years may be associated with a major viscosa (Swaileh et al. 2004), Rumex acetosa L. (Malinowska et new form of environmental pollution (Li et al. 2010). al. 2015), or Vicia cracca L. (Modlingerová et al. 2012). In the Potentially, this increase may pose a threat to both plant above mentioned but also other papers, with the exception of (REEs are not nutritionally essential for plants) and human PGE, the same elements (Cd, Cr, Cu, Pb, and Zn) have been health (Thomas et al. 2014), mainly as regards the intensity analyzed in different plant species. Among numerous herbaceous of use of these elements in new technologies (rechargeable species, Taraxacum officinale (Keane et al. 2001)and Achillea batteries, cell phones, or carbon arc lighting). millefolium L. (Modlingerová et al. 2012) have been the most For this reason, the aim of the study was to estimate the frequently analyzed. However, to date the phytoremediative po- phytoextraction efficiency of REEs in organs and whole bio- tential of Artemisia vulgaris L. and Trifolium repens L. have been mass of three herbaceous plant species: Artemisia vulgaris L., estimated only for As, Cd, Cu, Ni, Pb, and Zn (Kafoor and Kasra Taraxacum officinale F. H. Wigg., and Trifolium repens L. 2014; Çolak et al. 2016); Cu, Hg, and Pb (Pivić et al. 2013); As, naturally growing at three different distances (1, 10, and Cd, Cr, Cu, Mo, Ni, Pb, and Zn (Modlingerová et al. 2012); or 25 m) from the edge of a road (traffic lane). This paper is a As, Pb and Sb (Álvarez-Ayuso et al. 2012). development of studies described in our previous studies In literature, there are no studies that describe the concen- (Mikołajczak et al. 2017) with new data about the efficiency tration of REEs in Artemisia vulgaris L. and Trifolium repens of phytoextraction and distribution of REEs in organs of select- L., herbaceous plant species that commonly grow near roads. ed herbaceous plant species growing near the frequented road. Owing to significant difficulties in the proper analysis of REEs, the majority of scientific papers have been limited to the selec- tion of a few of them only (usually lanthanum (La) and/or neodymium (Nd)) (Diatloff et al. 2008; Lyubomirova et al. Materials and methods 2011;Siwulski etal. 2017). In recent years, accumulation of REEs has been mainly estimated in some plant species or in Characteristics of experimental material and its wild growing mushroom species (Mleczek et al. 2016a,b; Saatz collection et al. 2015; Zhang et al. 2015). Li et al. (2013) pointed out that the intake of vegetables in the vicinity of a large-scale mining Experimental materials were three herbaceous plant species: area is not related with exceeding the daily intake of REEs Artemisia vulgaris L., Taraxacum officinale F. H. Wigg., and 1 −1 (100–110 μgkg d ) but long-term exposure to these elements Trifolium repens L. (Table 1), growing near the S11, a road in food can be a real health risk. The path of REEs accumula- located in the central part of the Wielkopolska Region (52° 14′ tion together with a determination of the role of key ligands has 40.07″ N17° 07′ 28.02 E) (Fig. 1). Table 1 Characteristics of analyzed herbaceous plant species No. 1 2 3 Plant species A. vulgaris L. T. officinale F. H. Wigg. T. repens L. Common name common wormwood, mugwort dandelion white clover EPPO code ARTVU TAROF TRFRE Family Asteraceae Asteraceae Fabaceae Occurrence Present at uncultivated areas, roadsides The native species to Asia and Europe; The moist temperature zones; Australasia, or places of wastes landfill. present in North and South America Europe, Japan, North America, southern Asia, Europe, northern Africa, and southern Africa and Australia Latin America, North America Season of growth Flowering between July and October Flowering between April and July Late spring and summer (flowering between May and November) High [cm] 60–120 5–40 7–20 Leaves Sessile and pinnate dark green, Oblanceolate or obovate in shape, Trifoliate, elliptic and smooth, 1–2cmlong 5–15 cm long 3–35 cm long Environ Sci Pollut Res (2018) 25:23695–23711 23697 Fig. 1 Location of experimental site and method of sample collection Fifteen specimens of each plant species and soil samples while in 2016: W, SW, E, and NE (31.6; 15.7; 13.5; 11.4%, around the plants were collected along this road (50 m) from respectively). Meteorological data were obtained from the three distances from the edge of the road: 1, 10, and 25 m. monitoring station of the Institute of Meteorology and Soil samples were collected from 0 to 15 cm depth. Based on Water Management in Poznań. the interpretation of the content of the soil-agricultural map, it Whole plants were dug up using a polypropylene sample can be concluded that the investigations were carried out on spade so as to ensure roots were not damaged (cut). All ma- Luvisols, characterized by a loamy sand texture up to a depth terials were transported to the laboratory immediately after of about 75 cm and sandy loam texture in the underlying plant and soil sample collection. It is the common presence horizons (IUSS Working Group WRB 2015). According to of these three plant species in the vicinity of roads and the very Aide and Aide (2012), REE content in this soil type is lower limited data about their abilities for REE phytoextraction that than other soil types; hence, the anthropogenic sources had makes them highly suitable for the purpose of this study. the strongest effect on REE accumulation in soils and plants. All experimental materials were collected from two sides Preparation of samples (north and south) of the road and twice, on 12 August, 2015, in drought conditions after a period of 13 days without After transport to laboratory, each plant was carefully washed rainfall, and 13 August, 2016, after some rainy days. Total with deionized water using Milli-Q Advantage A10 Water rainfall within the 14 days before the plant material collection Purification Systems, Merck Millipore (Merck, Darmstadt, day in 2015 and 2016 was 1.2 and 27.7 mm, respectively. It is Germany) to remove traffic dust (leaves and stem) and soil worth noting that the total rainfall between 1 June and 12 particles (roots). Collected plants were divided into roots, August, 2015, and 1 June and 13, August, 2016, was 176.5 stem, and leaves, dried in an electric oven (TC 100, and 224.7 mm, respectively, which indicates differing water SalvisLAB, Switzerland) at 105 ± 3 °C for 96 h and ground conditions for plant growth. Mean temperatures within the for 3 min in a Cutting Mill SM 200 (Retsch GmbH, Haan, growing season in 2015 and 2016 were 14.5 and 15.5 °C, Germany). Three samples prepared for each plant organ of −1 respectively, and mean wind speed was 1.5 and 1.7 m s . three herbaceous plant species were digested using the micro- The wind direction varied in the 2 years of the study. In 2015, wave mineralization system CEM Mars 5 Xpress (CEM, the dominant wind directions were W, SW, E, NE, N and, Matthews, NC, USA). Prepared samples (0.3000 ± 0.0001 g) NW (34.2; 12.1; 10.5; 11.4; 10.0 and 9.8%, respectively), were placed in 55 mL vessels with 8 mL of concentrated 23698 Environ Sci Pollut Res (2018) 25:23695–23711 −1 Table 2 Characteristics of rare earth element concentration [mg kg ] (65%) HNO Suprapur® (Merck, Darmstadt, Germany) and and selected parameters of soil collected from three distances from the 1mLofH O for ultratrace analysis (Merck, Darmstadt, 2 2 edge of the road Germany) and digested according to a temperature program Element Unit 1 m 10 m 25 m that consisted of three stages: first stage: temperature 80 °C, time 10 min, power 600 W; second stage: temperature 120 °C, LREEs time 10 min, power 1200 W; third stage: temperature 200 °C, −1 a a b Ce mg kg 18.00 ±1.23 16.31 ±1.33 8.97 ±1.01 time 12 min, power 1600 W. After digestion, the solutions a a b Eu 0.15 ±0.02 0.13 ± 0.01 0.08 ±0.02 were filtrated using Qualitative Filter Papers (Whatman, a ab b Gd 1.54 ±0.15 1.31 ± 0.17 1.11 ± 0.09 Grade 595 4–7 μm) and filled with deionized water Milli-Q a a b La 3.86 ±0.28 3.35 ± 0.29 2.66 ±0.13 Advantage A10 Water Purification Systems, Merck Millipore a a b Nd 12.65 ± 0.97 11.96 ± 1.07 8.04 ±0.85 (Merck, Darmstadt, Germany) to a final volume of 50 mL. a ab b −1 Pr 0.86 ±0.12 0.81 ± 0.09 0.67 ±0.12 Concentrations of rare earth elements are expressed in mg kg a a b Sm 0.03 ±0.01 0.03 ± 0.01 0.01 ±0.00 of dry matter (d.m.) of plant organs, both in tables and the HREEs whole text. −1 a ab b Dy mg kg 0.56 ±0.11 0.52 ± 0.09 0.41 ±0.06 The preparation of soil samples followed the same proce- a ab b Er 47.21 ±4.19 40.87 ± 4.82 36.99 ±3.61 dure as the plant material. The only difference being that be- a a b Ho 0.04 ±0.01 0.03 ± 0.01 0.01 ±0.01 fore separate digestion with concentrated (65%) HNO a ab b Lu 0.15 ±0.03 0.13 ± 0.02 0.09 ±0.02 Suprapur® the samples were submitted to mercerization for a a a Sc 0.71 ±0.16 0.62 ± 0.12 0.58 ±0.13 24 h and the times of particular stages of digestion were twice a a b Tb 0.23 ±0.04 0.18 ± 0.02 0.13 ±0.01 as long with the same temperature and power. Soil samples a a a Tm 1.05 ±0.21 0.91 ± 0.11 0.88 ±0.09 were also characterized by pH (PN-ISO 10390:1997) and re- a ab b Y2.24 ±0.25 2.03 ± 0.18 1.79 ±0.16 dox potential (ISO 11271:2002) using a Microprocessor pH a a b Yb 0.34 ±0.06 0.29 ± 0.03 0.18 ±0.02 Meter 211 by Hanna Instruments and electrolytic conduction Chemical characteristics of soil (PN-ISO 1265+AC1:1997) using an EC-meter HI 2316 by a a a Ca % 0.103 ± 0.009 0.099 ± 0.008 0.098 ±0.011 Hanna Instruments (Woonsocket, Rhode Island, USA). a a b Chemical characteristics of soil are presented in Table 2. K % 0.116 ± 0.017 0.105 ± 0.011 0.078 ±0.009 a a a Mg % 0.105 ± 0.029 0.113 ± 0.015 0.102 ±0.018 The obtained results have shown a general decrease in the a a a majority of REEs with the distance from the edge of the road Na % 0.018 ± 0.005 0.019 ± 0.002 0.017 ±0.005 a a a (significant differences in mineral characteristics between soil P % 0.039 ± 0.010 0.042 ± 0.008 0.039 ±0.004 a a a samples collected from 1 and 25 m from the road). There were S % 0.018 ± 0.003 0.017 ± 0.001 0.017 ±0.002 a a a no significant differences between pH and EC values charac- Fe % 0.508 ± 0.028 0.479 ± 0.033 0.503 ±0.041 −1 a a a terized in the studied soil samples. Significant differences Mn mg kg 131 ±19 125 ± 6 128 ±9 a a a were only observed in Eh values between soils collected from pH – 6.03 ±0.09 6.05 ± 0.03 6.00 ±0.05 −1 a a a 10 and 25 m of the road. This was probably an effect of the EC μScm 608 ±12 579 ±27 593 ±24 ab b a shallow ground depressions found in this area, where rain Eh mV 203 ±13 185 ±12 210 ±7 water was accumulated, as well as differences in soil granula- n = 15, mean values ± SD; identical letters (a, b, c...) followed by values tion and soil humidity, as confirmed by the different allocation denote no significant (p = 0.05) difference in rows (for particular element of plants in this area. or soil parameter) according to Tukey’s HSD test (ANOVA); bDL below Detection Limit Analytical methods 442.434 nm, Tb 350.914 nm, Tm 336.261 nm, Y The determination of REEs was carried out using inductively 361.104 nm, and Yb 328.937 nm. The ICP-OES instrument coupled plasma optical emission spectrometry (ICP-OES) with did not allow the determination of promethium, which is a an Agilent 5100 (Agilent, Santa Clara, USA) spectrometer with man-made, radioactive element and is not recognized among a synchronous (dual axial and radial plasma) view. The follow- naturally occurring lanthanides. ing common instrumental parameters were used for determina- The detection limits were estimated at the level of 0.0X tion of all elements: RF power 1.2 kW, plasma gas (argon) flow −1 −1 −1 −1 −1 mg kg : for Ce 0.02 mg kg ,0.05mg kg for Dy, 12 L min , nebulizer gas (argon) flow 0.7 L min ,and radial −1 −1 −1 0.04 mg kg for Er, 0.07 mg kg for Eu, 0.07 mg kg for view height 8 mm. The following wavelengths were used for −1 −1 −1 Gd, 0.06 mg kg for Ho, 0.02 mg kg for La, 0.06 mg kg REE determination: Ce 446.021 nm, Dy 400.045 nm, Er −1 −1 −1 for Lu, 0.02 mg kg for Nd, 0.06 mg kg for Pr, 0.05 mg kg 349.910 nm, Eu 420.504 nm, Gd 342.246 nm, Ho −1 −1 −1 for Sc, 0.05 mg kg for Sm, 0.04 mg kg for Tb, 0.06 mg kg 348.484 nm, La 333.749 nm, Lu 307.760 nm, Nd −1 −1 for Tm, 0.04 mg kg for Y, and 0.03 mg kg for Yb, 406.108 nm, Pr 417.939 nm, Sc 361.383 nm, Sm Environ Sci Pollut Res (2018) 25:23695–23711 23699 respectively. The uncertainty was estimated on the level of from the traffic lane were also calculated. Additionally, −1 20% (k = 2) for the whole analytical procedure. the concentration of REEs [mg kg ] allowed the partic- The certified standard material CRM NCSDC 73349 ular element contents in whole plants biomass to be cal- (CNACIS, Beijing, China)—bush branches and leaves was culated [mg per plant]. used in traceability control. The recovery values were as fol- lows: Ce 119%, Dy 77%, Eu 77%, Gd 105%, Ho 82%, La 87%, Lu 91%, Nd 110%, Pr 83%, Sm 118%, and Yb 79%, respectively. For uncertified elements Er and Sc, an analysis of Results the certified standard material CRM 667 sediment (IRRM, Geel, Belgium) was additionally provided. The obtained re- The results described in this paper are the mean values calcu- coveries were Er 105% and Sc 107%. Recovery values in the lated for the parameters characterizing the materials collected range of 75–125% were recognized as satisfactory. in the first (2015) year of the 2-year studies (2015–2016) in the environment. The same relationships were found in the Statistical analysis and calculations phytoextraction of LREEs, HREEs, and REEs by organs of the three studied herbaceous plant species in 2015 and 2016. All statistical analyses were made using the agricole pack- With respect to the differing amount of rainfall in particular age (R). Estimation of the concentration of REEs, LREEs, years of studies, it is likely that the differences in the level of or HREEs (dependent variable) in organs of herbaceous these groups of elements were only observed. plant species (independent variable) was carried out. The mean of element concentration in particular plant species was compared. One-way analysis ANOVA with the F- Data selection Fisher test (α=0.05) wasusedtoverify the generalhy- pothesis with respect to the equality of the mean concen- Figure 2 presents the distribution and concentration of all tration of particular LREEs or HREEs in the analyzed three groups of elements in herbaceous plant species plant species. In the case of a null hypothesis being growing on two sides of a frequented road. The relation- rejected, the Tukey test for multiple comparisons was ap- ships between phytoextraction of LREEs and REEs were plied to divide the studied herbaceous plant species into almost the same between plant species with clear differ- homogenous groups (α = 0.05). ences in element concentration in plants growing on the For a graphical presentation of the similarities and dif- north and south side of the road. ferences between particular plant species growing at dif- The dominant wind direction in the 2 years of study was ferent distances from the road with respect to their west. In the case of the rest of each year, northwest and south- phytoextraction abilities for particular LREEs or HREEs west winds were observed, which could suggest that plants separately or all REEs, LREEs, or HREEs in the whole growing on both sides of the road should be characterized by a plant bodies, a heatmap analysis was performed. Two- similar concentration of REEs in their organs. We confirmed dimensional variables (plant species growing at different this relationship and the differences described in Fig. 2 could distances and REE concentration) were represented as be an effect of variable wind directions. blue colors. In spite of the fact that in both 2015 and 2016 the same To show significant differences between tested plants as relationship of LREE, HREE, and REE phytoextraction regards the concentration of all 16 REEs jointly in their efficiency between the studied plant species was recorded, whole biomass, the Friedman rank sum test was applied some differences between years were clearly observed. with pairwise comparisons using the Nemenyi multiple Phytoextraction of all three groups of elements in 2015 comparison test (posthoc.friedman.nemenyi.test) with q was lower than in 2016 which was probably the effect of approximation for unreplicated blocked data. the better growth conditions in the last year (the higher Additionally, to illustrate the potential of the analyzed number of rainy days). Concentration of REEs in A. plants in the phytoextraction of all 16 REE elements joint- vulgaris L. roots, stems, and leaves in 2016 was higher ly, the rank sum was performed. than that in 2015 with 13–21, 22–29, and 29–36%, respec- To estimate the efficiency of REE phytoextraction by tively. In the case of the T. officinale and T. repens,these the studied plant species, bioconcentration factor (BCF) increases were 8–14 and 15–19%, respectively, in roots values were calculated as the ratio of the concentration and 14–22 and 18–27%, respectively, in stem, while 13– of HREEs, LREEs, or REEs in the harvested organs 18 and 20–28%, respectively, in leaves. The presentation (leaves and stems) to their concentration in soil (Ali et of the 2015 results only was advisable to make the presen- al. 2013). Correlation coefficient (r) values between the tation of the abundant data clearer, especially as the same concentration of LREEs, HREEs, REEs, and distances relationships were observed between the plants. 23700 Environ Sci Pollut Res (2018) 25:23695–23711 −1 Fig. 2 Distribution and concentration [mg kg ] of REEs, LREEs, and HREEs in Artemisia vulgaris L. (a), Taraxacum officinale (b), and Trifolium repens L. (c) growing on north and south side and with respect to their distance from the traffic lane Concentration of light, heavy, and total rare earth 1or 10 m and25m from theroad. Inthe caseof thefirst, elements the following relationship was observed for concentration of LREEs (T. officinale L. stem, T. repens L. roots and The concentration of rare earth elements was diverse for stem), HREEs (A. vulgaris L. roots and leaves, T. officinale organs of all three plant species growing at 1, 10, and L. roots and stem), and REEs (A. vulgaris L. roots; T. 25 m distance from the edge of the road (Table 3). officinale roots, stems, and leaves; T. repens L. leaves). In Generally, concentration of REEs, HREEs, and LREEs in the second case, a similarity of element concentration were plant organs decreased with the distance from the road. observed for in two plants growing nearest the road with a Significant differences (p = 0.05) between the concentra- significantly lower concentration in plants from 25 m: tion of these three groups of elements were recorded in LREEs (A. vulgaris stem, T. officinale roots and leaves, selected organs of plants growing: (i) at distance 1 and and also T. repens L. roots), HREEs (A. vulgaris L. roots, 10 mor25 m andalso(ii) plants growing at a distance of T. officinale leaves and T. repens L. roots), and REEs (A. Environ Sci Pollut Res (2018) 25:23695–23711 23701 −1 Table 3 Concentration [mg kg d.m.] of light, heavy and total rare earth elements in organs of herbaceous plant species in different distance from the edge of the road Plant species Distance from Plant organ LREEs HREEs REEs the road b b b Artemisia vulgaris L. 25 m Root 11.26 ± 1.95 0.62 ± 0.10 11.88 ±2.03 ab b b 10 m 13.60 ± 1.62 1.03 ±0.10 14.63 ±1.63 a a a 1 m 19.66 ±2.77 4.03 ±0.46 23.69 ±2.88 F, p value 8.02, < 0.05 89.08, < 0.05 15.17, < 0.05 b b b 25 m Stem 8.82 ±0.64 0.51 ±0.16 9.33 ±0.54 a a a 10 m 18.65 ±2.74 1.08 ±0.17 19.73 ±2.90 a ab a 1 m 26.44 ±4.09 0.98 ± 0.15 27.42 ±3.98 F, p value 18.95, < 0.05 7.34, < 0.05 20.15, < 0.05 b b b 25 m Leaves 23.84 ±2.08 1.94 ±0.74 25.79 ±2.18 ab b ab 10 m 37.38 ± 3.69 2.07 ±0.34 39.45 ±3.36 a a a 1 m 56.21 ± 16.24 5.97 ±0.90 62.19 ±15.99 F, p value 5.63, < 0.05 21.38, < 0.05 7.46, < 0.05 b b c Taraxacum officinale 25 m Root 11.46 ± 1.62 1.53 ±0.28 12.99 ±1.67 a b b 10 m 22.20 ±2.16 1.97 ±0.20 24.17 ±2.14 a a a 1 m 27.83 ±2.88 3.08 ±0.46 30.90 ±2.59 F, p value 26.59, < 0.05 11.68, < 0.05 34.87, < 0.05 b b b 25 m Stem 26.85 ±2.77 1.31 ±0.14 28.16 ±2.65 b b b 10 m 31.61 ±0.89 1.99 ±0.13 33.61 ±1.00 a a a 1 m 40.86 ±3.98 3.47 ±0.78 44.32 ±3.93 F, p value 12.51, < 0.05 11.42, < 0.05 17.32, < 0.05 b b c 25 m Leaves 29.72 ±3.67 0.78 ±0.11 30.50 ±3.70 a a b 10 m 45.01 ±3.75 7.98 ±1.21 52.99 ±3.91 a a a 1 m 55.20 ± 14.44 10.44 ±1.39 65.64 ±15.79 F, p value 4.18, 0.07 44.34, < 0.05 6.82, < 0.05 b b b Trifolium repens L. 25 m Root 15.90 ±0.71 6.17 ±0.16 22.07 ±0.58 a a a 10 m 38.54 ±3.83 12.45 ±1.42 50.99 ±3.13 a a a 1 m 40.27 ±2.94 13.50 ±2.07 53.77 ±3.52 F, p value 46.61, < 0.05 14.87, < 0.05 82.08, < 0.05 b b b 25 m Stem 30.77 ±4.73 4.78 ±1.03 35.56 ±5.67 b ab ab 10 m 32.81 ±1.68 8.60 ± 2.27 41.41 ±1.70 a a a 1 m 39.15 ±1.88 10.29 ±1.13 49.44 ±0.75 F, p value 3.99, p < 0.05 6.39, < 0.05 8.18, < 0.05 b b b 25 m Leaves 22.50 ±2.06 2.57 ±0.26 25.06 ±2.31 b ab b 10 m 25.28 ±0.99 5.88 ± 1.13 31.16 ±2.08 a a a 1 m 42.56 ±2.93 8.88 ±2.59 51.44 ±5.23 F, p value 51.44, < 0.05 7.44, < 0.05 30.92, < 0.05 n = 15, mean values ± SD; identical letters (a, b, c...) followed by values denote no significant (p = 0.05) difference in columns (for particular organs and plant species) according to Tukey’sHSD test (ANOVA) vulgaris and T. repens L. roots). It is worth noting that for LREEs in the sum of REEs). For A. vulgarsis L. and T. A. vulgaris L. roots (LREEs), leaves (LREEs and REEs), T. officinale, the highest concentration of LREEs, HREEs, and repens L. stems (HREEs and REEs), and leaves (HREEs), REEs was observed in leaves while for T. repens L. the con- significant differences between the concentration of ele- centration of all element groups was more uniform in the ments in particular groups in plants growing at a distance whole plant biomass. of 1 and 25 m from the road were also observed. To show the efficiency of REE phytoextraction, LREEs formed the main component of REEs concentration bioconcentration factor (BCF) values were calculated (Table (significantly lower concentration of HREEs than that of 4). Only for LREEs, was the BCF > 1 observed for all plant 23702 Environ Sci Pollut Res (2018) 25:23695–23711 Table 4 Bioconcentration factor (BCF) values of LREEs, HREEs, and In the rest of cases, concentrations of LREEs in plant or- REEs with correlation coefficient (r)values gans were usually significantly different between plants grow- ing at 1 and 15 m, while there were no significantly different Plant species Distance from the road LREEs HREEs REEs concentrations between plants from 1 and 10 m or 10 and A. vulgaris L 25 m 1.52 0.06 0.56 25 m. It is worth emphasizing that the concentration of Gd 10 m 1.65 0.07 0.74 in A. vulgaris L. stem, Pr in T. officinale stem, and Sm in T. 1 m 2.23 0.13 1.01 repens L. roots and leaves was significantly higher in plants r 0.9338 0.9672 0.9780 growing at 25 m than 10 m with similar values to plants T. officinale 25 m 2.63 0.05 0.94 growing 1 m from the edge of the road. This observation 10 m 2.26 0.22 1.09 suggests that particular LREEs are accumulated and 1 m 2.59 0.26 1.23 transported to aerial parts in a way that is characteristic for r 0.9495 0.9515 0.9958 these plants, which is generally not related to the same trend T. repens L. 25 m 2.47 0.18 0.97 observed for the sum of LREEs (decrease of their 10 m 1.71 0.32 0.91 phytoextraction with distance from the road). 1 m 2.20 0.36 1.13 Differences in LREEs concentration was especially visible r 0.7695 0.9711 0.9311 in the roots of A. vulgaris L. and T. repens L., although no significant differences were observed between the concentra- tions of Pr in plants growing at different distances from the species, regardless of distance from the edge of the road. The road. The highest concentration of LREEs was stated for Nd. opposite situation was recorded for HREEs, while in the case Only for this element was significant differences observed for of the REEs, BCF > 1 was found for all plant species growing all organs of the three plant species in relation to distance from at the 1-m distance from the road (from BCF = 1.23 for T. the road, with the exception of T. repens L. stems. Nd and Ce officinale to BCF = 1.01 for A. vulgaris L.) and also T. were two dominant LREEs present in the tested plant species. officinale growing 10 m from the road only (BCF = 1.09). No significant differences in concentration of Ho, Lu, Tb, Moreover, a decrease of the BCF with an increase of the dis- and Yb in organs of all plants growing at 1, 10, and 25 m from tance from the road was observed for phytoextraction of the road were observed with the exception of Tb in A. vulgaris LREEs, HREEs and REEs by A. vulgaris L., HREEs and L. leaves and T. officinale roots and also Yb in A. vulgaris L. REEs by T. officinale, and also HREEs by T. repens L. stems and T. repens L. leaves. For Dy, Sc, and Tm, there were no significant differences for A. vulgaris L. and T. officinale organs collected from particular distances from the road. The Concentration of particular light and heavy rare earth same relationships for Y concentration in A. vulgaris L. stems elements and T. officinale roots and stems were recorded. A dominant HREE characterized by significantly higher concentration in Characteristics of LREEs in the organs of the three herbaceous the studied plant species organs growing at a distance of 1 m plant species are presented in Table 5. There were no signifi- from the road was Er. Concentration of Er was generally uni- cant differences between the concentration of these elements form in T. repens L. organs, whereas in the other plant species, in plant organs and the distance from the road, especially for this element was effectively transported to the leaves. In the A. vulgaris L. (Pr in roots; Eu and Sm in stems; and also Ce, group of HREEs, the lowest diversity was observed for Ho, Eu, Pr, and Sm in leaves); T. officinale (Ce, Eu, Gd, and La in Lu, Tm, Yb, Sc, and Tb, mainly in T. officinale and T. repens roots; Ce, Eu, Gd, La, and Sm in stems; and also Ce, Eu, Pr, L. organs. For this reason, it is interesting to note that the and Sm in leaves); and T. repens L. (Pr in roots; Ce, Eu, Nd, tendency described for HREEs related with a decrease in their Pr, and Sm in stems; and Ce, Eu, Gd, and La in leaves). A concentration in plant organs with the distance from the road significant difference between the concentration of selected was an effect of Er concentration. LREEs in plant organs from 1 m and 10 or 25 m were ob- served for Ce, Eu, and Sm in A. vulgaris roots; Nd and La in Comparison of REEs phytoextraction in whole plant stems and leaves, respectively. The same relationships were biomass recorded for Gd in stems and Nd in leaves of T. repens L. Additionally, a similar concentration of particular LREEs in Estimation of phytoextraction efficiency can be confirmed by organs of plants from a distance of 1 and 10 m from the road taking plant biomass into consideration to show how great an with simultaneous significantly lower concentration in plants amount of element was accumulated in the whole plant bio- from 25 m were observed for Gd in A. vulgaris L. leaves, Nd mass (Table 6). and Pr in roots and Nd in T. officinale leaves, and also Ce, Gd, The data presented in Table 6 confirm that the content of La, and Nd in T. repens L. roots. elements belonging to LREEs, HREEs and REEs decreased Environ Sci Pollut Res (2018) 25:23695–23711 23703 −1 Table 5 Concentration [mg kg ] of particular light rare earth elements in organs of herbaceous plant species in different distance from the edge of the road Plant species Distance from Plant organ Ce Eu Gd La Nd Pr Sm the road b b ab b b a b Artemisia vulgaris L. 25 m Root 2.18 0.04 0.11 0.34 7.54 1.05 0.01 b b a a ab a b 10 m 1.90 0.04 0.15 0.86 9.85 0.79 0.01 a a b b a a a 1 m 5.51 0.08 0.04 0.26 13.03 0.71 0.04 F,p value 13.67 8.00 6.59 12.16 5.04 1.78 9.14 <0.05 <0.05 <0.05 <0.05 <0.05 0.25 <0.05 b a a b b b a 25 m Stem 1.61 0.04 0.15 0.08 6.71 0.23 0.01 a a b a b a a 10 m 4.65 0.04 0.08 0.15 12.90 0.83 0.01 ab a b b a b a 1 m 3.15 0.08 0.04 0.08 23.03 0.04 0.04 F, p value 18.35 4.80 18.98 8.20 16.07 43.47 4.92 <0.05 0.06 <0.05 <0.05 <0.05 <0.05 0.05 a a b b b a a 25 m Leaves 5.06 0.08 0.04 0.19 17.61 0.86 0.01 a a a b ab a a 10 m 5.08 0.04 0.15 0.51 30.79 0.81 0.01 a a a a a a a 1 m 6.53 0.08 0.15 0.68 47.55 1.20 0.04 F, p value 0.69 < 0.05 4.36 17.25 5.29 6.09 1.75 4.92 0.07 <0.05 <0.05 <0.05 0.25 0.05 a a a a b b b Taraxacum officinale 25 m Root 3.19 0.04 0.08 0.49 6.95 0.71 0.01 a a a a a a ab 10 m 4.54 0.04 0.08 0.49 15.94 1.09 0.04 a a a a a a a 1 m 5.18 0.08 0.08 0.56 20.55 1.31 0.08 F, p value 2.83 3.43 0.00 0.71 23.41 2.83 10.48 0.14 0.10 1.00 0.53 <0.05 0.14 <0.05 a a a a b a a 25 m Stem 4.99 0.04 0.04 0.26 20.20 1.31 0.01 a a a a ab b a 10 m 4.80 0.04 0.04 0.30 25.91 0.49 0.04 a a a a a a a 1m 6.11 0.08 0.08 0.34 32.72 1.50 0.04 F, p value 1.32 6.00 3.69 0.33 13.44 12.10 4.57 0.34 <0.05 0.09 0.73 <0.05 <0.05 0.06 a a b b b a a 25 m Leaves 4.73 0.02 0.04 0.23 23.24 1.46 0.01 a a ab ab a a a 10 m 5.74 0.04 0.08 0.41 37.58 1.13 0.04 a a a a a a a 1 m 5.85 0.04 0.11 0.45 46.80 1.88 0.08 F, p value 1.10 0.59 5.75 6.92 3.71 2.43 1.73 0.39 0.58 <0.05 <0.05 0.09 0.17 0.26 b b b b b a a Trifolium repens L. 25 m Root 4.43 0.04 0.08 0.34 10.31 0.64 0.08 a a a a a a b 10 m 9.64 0.11 0.64 1.99 25.21 0.94 0.02 a ab a a a a ab 1 m 10.84 0.08 0.60 2.21 25.31 1.20 0.04 F,p value 9.77 10.18 8.93 14.27 24.13 3.98 7.16 <0.05 <0.05 <0.05 <0.05 <0.05 0.08 <0.05 a a c b a a a 25 m Stem 5.25 0.04 0.04 0.26 24.25 0.86 0.08 a a b ab a a a 10 m 6.15 0.08 0.23 0.71 23.85 1.76 0.04 a a a a a a a 1 m 7.84 0.04 0.38 1.24 27.60 2.03 0.04 F, p value 4.09 6.00 25.87 9.92 0.92 2.90 2.67 0.08 <0.05 <0.05 <0.05 <0.45 0.13 0.15 a a a a b b a 25 m Leaves 4.65 0.04 0.04 0.15 17.02 0.49 0.11 a a a a b ab b 10 m 6.04 0.04 0.15 0.64 17.51 0.86 0.05 a a a a a a b 1 m 7.05 0.08 0.23 1.13 32.93 1.13 0.04 F, p value 2.32 1.71 3.17 4.16 19.58 10.06 9.77 0.18 0.26 0.12 0.07 <0.05 <0.05 <0.05 n = 15, mean values ± SD; identical letters (a, b, c...) followed by values denote no significant (p = 0.05) difference in columns (for particular organs and plant species) according to Tukey’sHSD test (ANOVA) 23704 Environ Sci Pollut Res (2018) 25:23695–23711 −1 Table 6 Concentration [mg kg ] of particular heavy rare earth elements in organs of herbaceous plant species in different distance from the edge of the road Plant species Distance from Plant organ Dy Er Ho Lu Sc Tb Tm Y Yb the road a b a a a a a b a Artemisia vulgaris L 25 m Root 0.01 0.30 0.01 0.01 0.04 0.01 0.04 0.19 0.01 a b a a a a a b a 10 m 0.01 0.64 0.04 0.04 0.04 0.01 0.04 0.19 0.04 a a a a a a a a a 1 m 0.01 3.12 0.04 0.04 0.08 0.04 0.11 0.56 0.04 F, p value 0.00 35.05 1.56 0.96 3.69 2.56 4.90 3.55 1.68 1.00 <0.05 0.28 0.43 0.09 0.16 0.05 0.10 0.26 a b a a a a a a b 25 m Stem 0.01 0.34 0.02 0.03 0.04 0.01 0.04 0.02 0.01 a a a a a a a a a 10 m 0.01 0.75 0.04 0.08 0.04 0.02 0.04 0.04 0.08 a ab a a a a a a a 1 m 0.01 0.60 0.04 0.08 0.04 0.04 0.04 0.05 0.09 F, p value 0.00 6.71 0.78 3.41 0.00 3.06 0.00 1.34 17.71 1.00 <0.05 0.50 0.10 1.00 0.12 1.00 0.33 <0.05 a b a a a b a b a 25 m Leaves 0.01 1.73 0.01 0.02 0.04 0.02 0.04 0.08 0.01 a b a a a b a a a 10 m 0.01 1.50 0.04 0.04 0.06 0.02 0.08 0.30 0.04 a a a a a a a a a 1 m 0.01 5.18 0.04 0.04 0.08 0.08 0.08 0.45 0.04 F 0.00 19.60 4.57 0.78 2.77 18.06 1.92 29.32 3.20 p value 1.00 <0.05 0.06 0.50 0.14 <0.05 0.23 <0.05 0.11 a b a a a b a a a Taraxacum officinale. 25 m Root 0.01 1.01 0.01 0.04 0.04 0.01 0.08 0.30 0.04 a ab a a a b a a a 10 m 0.01 1.50 0.04 0.04 0.04 0.01 0.04 0.26 0.04 a a a a a a a a a 1 m 0.01 2.37 0.04 0.06 0.08 0.04 0.08 0.38 0.04 F, p value 0.00 8.25 2.46 1.40 3.43 64.00 1.37 1.74 0.01 1.00 <0.05 0.17 0.32 0.10 <0.05 0.32 0.25 1.00 a b a a a b a a a 25 m Stem 0.01 1.01 0.01 0.04 0.04 0.01 0.04 0.11 0.04 a b a a a b a a a 10 m 0.01 1.58 0.04 0.06 0.04 0.01 0.04 0.19 0.04 a a a a a a a a a 1 m 0.01 2.98 0.04 0.06 0.04 0.04 0.08 0.19 0.04 F, p value 0.00 11.64 4.57 1.00 0.00 1.23 1.23 1.25 0.02 1.00 <0.05 0.06 0.42 1.00 0.36 0.36 0.35 0.98 a b a a a a a b a 25 m Leaves 0.01 0.45 0.01 0.04 0.08 0.01 0.04 0.11 0.04 a a a a a a a ab a 10 m 0.01 7.50 0.04 0.05 0.08 0.01 0.04 0.23 0.04 a a a a a a a a a 1 m 0.01 9.79 0.04 0.08 0.08 0.04 0.08 0.26 0.08 F, p value 0.00 44.10 2.46 2.18 0.00 4.92 1.50 7.44 2.67 1.00 <0.05 0.17 0.19 1.00 0.05 0.30 <0.05 0.15 b b a a b a b b a Trifolium repens L. 25 m Root 0.05 5.63 0.04 0.04 0.04 0.04 0.11 0.19 0.04 ab a a a a a a a a 10 m 0.11 10.02 0.03 0.08 0.34 0.04 0.38 1.43 0.04 a a a a a a a a a 1 m 0.15 11.06 0.04 0.08 0.30 0.08 0.38 1.35 0.08 F, p value 10.37 8.81 0.02 4.00 36.71 1.60 7.12 60.63 1.55 <0.05 <0.05 0.98 0.08 <0.05 0.28 <0.05 <0.05 0.29 b b a a b a b b a 25 m Stem 0.02 4.35 0.04 0.04 0.04 0.04 0.08 0.15 0.04 b ab a a a a a a a 10 m 0.04 7.05 0.05 0.04 0.19 0.04 0.26 0.90 0.04 a a a a ab a b ab a 1 m 0.14 9.25 0.04 0.04 0.11 0.04 0.11 0.49 0.08 F, p value 8.60 5.85 0.22 0.00 10.13 0.00 13.54 11.15 1.92 <0.05 <0.05 0.81 1.00 <0.05 1.00 <0.05 <0.05 0.23 b b a a b a a c b 25 m Leaves 0.02 2.29 0.04 0.04 0.04 0.04 0.04 0.04 0.04 b ab a a a a a b a 10 m 0.04 4.88 0.03 0.04 0.15 0.04 0.15 0.41 0.15 a a a a ab a a a a 1 m 0.14 7.65 0.04 0.04 0.08 0.04 0.11 0.64 0.15 F, p value 13.40 7.10 0.11 0.11 5.65 0.00 4.20 6.37 7.66 <0.05 <0.05 0.90 0.99 <0.05 1.00 0.07 <0.05 <0.05 n = 15, mean values ± SD; identical letters (a, b, c...) followed by values denote no significant (p = 0.05) difference in columns (for particular organs and plant species) according to Tukey’sHSD test (ANOVA) Environ Sci Pollut Res (2018) 25:23695–23711 23705 with the distance from the road. It is worth emphasizing that Characteristics of the heatmaps prepared separately for the results which show the content of REEs and LREEs in LREEs and HREEs are shown in Figs. 4 and 5. plants growing at 1, 10, and 25 m from the road suggest that The Friedman rank sum test determined some significant phytoextraction efficiency for these element groups was as differences with respect to the content of LREEs, HREEs, and follows: A. vulgaris L. > T. officinale ≥ T. repens L. In the REEs between the compared plant species growing at varying case of HREEs, the same relationships were not observed, distances from the road. In the case of LREEs, significant thus confirming the data presented in the heatmap (Fig. 3). differences were only observed between A. vulgaris L. and It is interesting to note that the color intensity (the darker T. repens L. growing 1 m from the road (Friedman chi- the higher the concentration of elements) of particular rectan- squared (χ ) = 8.8571; p value = 0.0119). For HREEs, sig- gles of both specific plants (Fig. 3a) and mean values (Fig. 3b) nificant differences between plant species growing at all three for LREEs and REEs was the same, which would indicate that distances were observed. In the case of 25 m, significant dif- for REEs the largest part of these elements is LREEs, whereas ferences between A. vulgaris L. and T. repens L. were con- HREEs comprise only an inconsiderable portion of the REEs. firmed (χ =7.5152, p value = 0.0233). At 1 and 10 m, sig- nificant differences between T. officinale and A. vulgaris L. and also between A. vulgaris L. and T. repens L. were ob- 2 2 served (χ =8.0741, p value = 0.0177 and χ = 13.273, p F F value = 0.00131, respectively, for plants collected from 1 and 10 m from the edge of the road). Significant differences between REEs content in A. vulgaris L. and T. repens (χ = 6.7458, p value = 0.0343) growing at a distance of 25 m from the road were noted. For Fig. 3 Correlation between herbaceous plant species collected from three Fig. 4 Correlation between herbaceous plant species collected from three distances from the road with respect to the concentration of REEs, distances from the road with respect to the concentration of particular HREEs and LREEs (Heatmap) in all collected specimens (a) and the LREEs (Heatmap) in all collected specimens (a) and the mean values mean values (b) with presentation of a hierarchical tree plot (b) with presentation of a hierarchical tree plot 23706 Environ Sci Pollut Res (2018) 25:23695–23711 Discussion The presence of trace toxic elements in the environment is a real ecological problem that can have a harmful influence on living organisms (Li et al. 2010;Pagano etal. 2015b). REEs are not described as potentially toxic for humans but their increasing use in new technologies and consequent transport to the environment may eventually lead to dangerous levels of concentration (Mleczek et al. 2017). Roads are only one of the sources of REEs (Kennedy and Mitchell Limited 2003), but owing to the high charge of pollutants that may be transferred to soil adjacent to roads (Djingova et al. 2003), it is necessary to find a definite solution to reduce the amount of REEs that accumulate nearby. One of the most promising ways is the phytoextraction of pollutants by plants growing near the road. Herbaceous plant species seem to be highly suitable for such purpose not only because of their common presence near roads but also because of their dense growth in population per area unit. Phytoextraction efficiency depends on many environmental factors, but we have shown that thanks to the high correlation coefficient values (r > 0.9300) between REE concentration in soil and plant organs, the concentration of these elements has—together with their concentration in road dust—a decisive influence on their accumulation in the stud- ied plants. The same observation was described by Carpenter et al. (2015), who have shown that phytoextraction of REEs increases in plant organs (especially in roots) with an increase of their concentration in soil. This relationship was shown by a Fig. 5 Correlation between herbaceous plant species collected from three distances from the road with respect to the concentration of particular hydroponic experiment of Saatz et al. (2015), where low con- HREEs (Heatmap) in all collected specimens (a)and the mean values −1 centrations of Gd and Y (0.1 and 1 mg L ) or a higher con- (b) with presentation of a hierarchical tree plot −1 centration of these metals (10 mg L ) used in nutritional plants growing 10 m from the road, there were significant solution were respectively unrelated with a negative, or were differences between A. vulgaris L. and T. repens L. and also the cause of insignificant influence to plant biomass. A. vulgaris L. and T. officinale (χ = 18.931, p value = Moreover, the response of plants growing under REEs de- −5 7.748e ). Differences between the same herbaceous plant pends on their concentration in soil and the kind of substrate species growing in direct proximity to the road (1 m) were (hydroponic, soil, wastes). We have also shown that REEs also observed (χ =16.036, p value = 0.000329). were accumulated mainly in roots but also in leaves of the In order to define the efficiency of particular analyzed herba- studied herbaceous plant species which indicates the high po- ceous plant species in the phytoextraction of LREEs, HREEs, tential of these elements for phytoextraction and translocation and REEs, the rank sum was performed. According to this anal- to aerial plant parts (Saatz et al. 2015). A plant characterized by ysis, the efficiency of LREE and REE phytoextraction in all high efficiency of REEs phytoextraction when growing in a tested plant bodies was as follows: A. vulgaris L. > T. officinale- hydroponic experiment, Zea mays studied by Saatz et al. > T. repens L. In the case of HREEs, the same relationship was (2016) was found to activate specific defense mechanisms. only observed for plants growing at a distance of 1 m. The authors reported an extremely high concentration of Gd −1 To show the relationship between the concentration of and Y (3.17 and 8.43 g kg , respectively) in the roots of the LREEs, HREEs, and REEs in soil and their total content in maize, which was gained thanks to the accumulation of these the studied plant species, the correlation coefficient factor elements at the epidermis thereby limiting the availability of values were calculated (Table 7). With the exception of the REEs and increasing the plants’ survivability. LREEs in the whole biomass of T. repens (r =0.7695), all r One problem of phytoextraction of REEs is usually related values were higher than 0.93, which interchangeably has with plant species and the amount of element concentrations shown that the concentration of these elements in soil plays in substrates (Zhuang et al. 2017), because only selected a significant role in phytoextraction of all three groups of plants are suitable for this purpose, as confirmed by Zhang elements by the analyzed plant species. andShan(2001) after fertilizer application. Chemical Environ Sci Pollut Res (2018) 25:23695–23711 23707 Table 7 Content [mg per plant] of rare earth elements in whole herbaceous plant species growing in three distances from the edge of the road Plant species Distance from Ce Eu Gd La Nd Pr Sm LREEs REEs the road b b a b b b b b c A. vulgaris L. 25 m 0.03229 0.00068 0.00245 0.00235 0.12702 0.00734 0.00018 0.17231 0.18242 a b b a b a b a b 10 m 0.07203 0.00066 0.00164 0.00546 0.22543 0.01440 0.00018 0.31980 0.33918 a a b b a b a a a 1 m 0.06601 0.00132 0.00072 0.00233 0.38167 0.00376 0.00066 0.45647 0.48759 a a a a c b c b b T. officinale 25 m 0.01877 0.00013 0.00022 0.00141 0.07547 0.00519 0.00004 0.10123 0.10625 a a a a b b b a b 10 m 0.02256 0.00016 0.00029 0.00181 0.12239 0.00428 0.00016 0.15166 0.17223 a a a a a a a a a 1 m 0.02496 0.00026 0.00040 0.00203 0.15387 0.00706 0.00029 0.18887 0.21733 a a b c b b a b b T. repens L. 25 m 0.01331 0.00010 0.00011 0.00051 0.05155 0.00163 0.00028 0.06750 0.07656 a a ab b b ab b b b 10 m 0.01724 0.00014 0.00052 0.00197 0.05385 0.00303 0.00012 0.07686 0.09579 a a a a a a b a a 1 m 0.02054 0.00018 0.00077 0.00332 0.08696 0.00376 0.00010 0.11563 0.14176 Plant species Distance from Dy Er Ho Lu Sc Tb Tm Y Yb HREEs the road a c a a a b a b b c 0.00653 0.00031 0.00040 0.00066 0.00018 0.00066 0.00102 0.00018 0.01011 A. vulgaris L. 25 m 0.00018 a b a a a b a b a b 10 m 0.00018 0.01320 0.00066 0.00116 0.00067 0.00032 0.00068 0.00135 0.00116 0.01938 a a a a a a a a a a 1 m 0.00018 0.02224 0.00066 0.00116 0.00082 0.00068 0.00096 0.00304 0.00138 0.03113 a b b a a b a b a c T. officinale 25 m 0.00004 0.00333 0.00004 0.00016 0.00024 0.00004 0.00022 0.00077 0.00017 0.00502 a a a a a b a ab a b 10 m 0.00004 0.01853 0.00016 0.00021 0.00024 0.00004 0.00016 0.00101 0.00016 0.02057 a a a a a a a a a a 1 m 0.00004 0.02567 0.00016 0.00030 0.00029 0.00016 0.00033 0.00124 0.00024 0.02845 b b a a b a b b b b T. repens L. 25 m 0.00006 0.00814 0.00010 0.00010 0.00010 0.00010 0.00014 0.00020 0.00010 0.00906 b ab a a a a a b a ab 10 m 0.00011 0.01560 0.00010 0.00011 0.00046 0.00010 0.00052 0.00159 0.00033 0.01893 a a a a ab a ab a a a 1 m 0.00039 0.02272 0.00010 0.00011 0.00026 0.00011 0.00034 0.00174 0.00036 0.02613 n = 15, mean values ± SD; identical letters (a, b, c...) followed by values denote no significant (p = 0.05) difference in columns (for particular plant species from different distance from the road) according to Tukey’sHSD test (ANOVA) characteristics of substrate and plant species can modulate its other elements present in soil, may be a factor that modulates response and phytoextraction of REEs (Saatz et al. 2015). An the higher or lower phytoextraction of particular REEs, which example can be differences in our observation in relation to could be another aspect influencing the accumulation of REEs the studies of Agnan et al. (2014), who have analyzed numer- as described, e.g., by Olivares et al. (2014). ous lichen and moss species. The ability of these plants to When comparing the concentration of particular REEs in phytoextract particular elements was as follows: Ce > La > soil andintheearth’s crust (EPA 2012), a significantly higher Nd > Pr > Sm > Gd > Dy > Er > Yb > Eu > Tb > Ho > Tm > concentration of Tm and Y was observed in the studied soil Lu. The same relationship between element concentration (La near the road. In the case of the rest of the REEs, their concen- > Nd > Gd > Er) was described by Wiche et al. (2017), who tration was many times lower than in the earth’scrust have analyzed REEs in Brassica napus, Hordeum vulgare, (Wedepohl 1995). The use of selected REEs such as Ce, La, and Zea mays. They have shown that the amount of bioavail- or Nd in automobile converter catalysts used to enhance pollut- able REEs is about 30% of their total concentration in the soil, ant oxidation, explains the high concentration, particularly of and the phytoextraction efficiency of these elements by plants La and Ce in road dust (Djingova et al. 2003) but also in soil can differ in moist and mesic grassland. This could explain the near frequented roads (Figueiredo et al. 2009;Mikołajczak et al. difference of these observations in relation to our studies, where 2017). Figueiredo et al. 2009 studied soils in 14 public parks of for the weed species, the efficiency of REE phytoextraction São Paulo and found the following concentration of elements: was Nd > Ce > Er > La> other elements, with some exceptions, Ce > La > Nd > Yb = Sm > Tb = Lu = Eu, while in our studied dependent on the distance from the road and the plant species. soil the concentration was as follows: Ce > Nd > La > Yb > Tb The stated differences could be the result of the varying bio- =Lu = Eu > Sm. The differences in the concentration of partic- availability of elements in soil near the frequented road or the ular REEs may be related not with density of traffic but the total element concentration in soils (Abechi et al. 2010; Adedeji natural geological composition of the soils. The concentration et al. 2013). Carpenter et al. (2015) described different of REEs in soil was different with respect to the distance from phytoextraction of particular REEs as regards their concentra- the road. This suggests the important role of traffic in soil con- tion in soil,e.g., Nd >Pr>rorPr>Nd >Erfor A. syrica roots tamination. In spite of the fact that some authors have found no andNd> Er >Pr or Nd >Pr > Erfor R. sativus roots. The concise correlation between REE concentrations in soil and mutual relationship between REEs, as well as the influence of plants (Tyler 2004; Wiche and Heilmeier, 2016), we have stated 23708 Environ Sci Pollut Res (2018) 25:23695–23711 such a relationship. It is likely that the differences between our elements (especially As, Cu, Pb, and Zn) were described by results and those of the above mentioned authors were due to Pivić et al. (2013), Modlingerová et al. (2012), or Çelenk and the amount of bioavailable forms of REEs and also the pH and Kiziloğlu (2015). The diverse efficiency of phytoextraction of Eh of soils which significantly influenced REE phytoextraction REEs could also be an effect of the changes in the physiology (Cao et al. 2000). In many cases, other authors have found the of these plants, such as the biosynthesis of selected low mo- same tendency in trace element deposition (Kafoor and Kasra lecular weight organic acids (LMWOAs), especially oxalic, 2014), where the concentration of bioavailable elements for acetic, and citric acids, excluded from the rhizosphere or the plants was lower the further away from the road (Çolak et al. creation of phenolic acids (salicylic acid) as a response to ox- 2016). Xinde et al. (2000) pointed out the necessity for chem- idative stress caused by trace element occurrence (unpublished ical fractionation and multiple regression analysis to estimate data for presented plant species). Wiche et al. (2017) the bioavailability of REEs and to indicate differences in the underlined recently the significant role of these acids, especial- bioavailability of particular species of REEs of individual ele- ly citric acid, as a factor increasing the mobility of REEs in soil ments. In our paper, such an analysis was not done; therefore, a and finally increasing that of the phytoextraction of this group crucial role is played by pH or redox potential (Cao et al. 2001) of elements. A. vulgaris L. was a species characterized by of soil related with mobility (or not) and electric conductivity, higher biomass of its root system able to effectively being an indicator of the presence of additional stress for plant phytoextract trace elements (also REEs), while the ability of (salinity). The pH of the soil analyzed in our experiment was T. officinale was lower and T. repens L. the lowest among the 6.00–6.05 with visible uptake of REEs confirmed by BCF > 1. studied plant species. The root systems of all the plant species Thomas et al. (2014) found clear differences in the were found at 0–15 cm depth, where characteristics of soils for phytoextraction of selected REEs (Ce, La, Y) by native plants growing at the same distance from the road were the Canadian plant species and commonly used crop species in same. For this reason, differences in the creation of selected terms of different pH values (4.08 and 6.74). A higher pH value LMWOAs by particular herbaceous plant species are respon- was related to a generally lower phytoextraction of REEs, sible for higher or lower phytoextraction of REEs, as previous- which suggests that the studied herbaceous plant species could ly described by Shan et al. (2003). Another important fact be able to uptake these elements more effectively in the case of relating to the diverse distribution of REEs in soils and more acidic soils. It is worth underlining that a small change in phytoextraction (Fig. 2) is that traffic is likely to be an impor- the pH of soil may be related with significant differences in tant source of REEs with limitation of their delivery to further REE phytoextraction, as described by Wiche et al. (2016). distances from the road (Li et al. 2010). The authors have shown that phytoextraction of La and Nd We know that the plants studied in this paper were able to was significantly higher in herbs than in grasses and REEs are phytoextract REEs but how efficient was this process in relation more effectively accumulated in slightly acidic than slightly to other plants? The described efficiency of REE phytoextraction alkaline soils. On the other hand, the results of the study by is significantly lower than that for hyperaccumulators such as Khan et al. (2017), whichanalyzedplantsofthe Cyperaceae, Dicropteris dichotoma (Shan et al. 2003), where concentration Gleicheniaceae,and Melastomataceae families and their poten- of La, Ce, Nd, and Pr was up to 0.7% of its dry leaf biomass. tial for phytoextraction of REEs, indicated that this process is Also Khan et al. (2017) have described potential of plant species also EC dependent. Moreover, lower pH and EC values were belonging to the Cyperaceae, Gleicheniaceae,and related to higher concentrations of, e.g., Ce and Y, while the Melastomataceae families to phytoextract REEs with very high concentration of, e.g., La and Sc was lower. This observation is values of BCF (12.4–151.7). The response of the selected plant similar to the relationships described by Thomas et al. (2014), species may be also be different as regards their specific envi- and it can explain the relationships observed in our studies. It is ronmental requirements, such as the amount of other trace ele- worth underlining that the higher salinity (higher EC values) in ments important for their growth, which in the case of REEs is our studies compared to those in the paper of Khan et al. (2017) especially important. Wang et al. (2008) studies on horseradish pointed to the high potential of the studied herbaceous plant have shown that there is a relationship between REEs and the species uptake of REEs from soils near roads. concentration of other trace elements. The growth of the studied We have shown that concentration of REEs (LREEs and herbaceous plant species near the frequented road with many HREEs) in soils decreased with distance from the road, and the other plant species had to be related to mutual interactions that same tendency was observed for the content of REEs in total modified the efficiency of REE uptake. The importance of the plant biomass. Interestingly, no such correlation was observed influence of such relationships (plant growth stimulation or in- for certain LREEs and the majority of HREEs. Wiche et al. hibition, synergism or antagonism between elements) both for (2017) have also found differences in the concentration of both REEs and many other elements and plants was shown by Wiche groups of elements in soil and, similarly to our results, the et al. (2016), Liu et al. (2017), or Drzewiecka et al. (2017). efficiency of the phytoextraction of LREEs was higher than Moreover, this relation can influence the growth conditions. that of HREEs. Very similar observations for many other AccordingtoChenetal. (2016), Dicranopteris dichotoma is a Environ Sci Pollut Res (2018) 25:23695–23711 23709 plant recommended for controlling REE migration which can be of REE phytoextraction by T. officinale F.H. Wigg and T. repens related with intensified phytoextraction of these elements just by L. in particular may be characteristic of the greater ability of this plant species. It is known that a low concentration of REEs these plant species in relation to other elements, as presented, in soil is usually related to plant growth stimulation, while high e.g., by Porębska and Ostrowska (1999). concentrations have a negative influence for both plant growth and phytoextraction of trace elements (Zhang et al. 2013), but there are limited data about the influence of all 17 REEs to plant Conclusion response (de Oliveira et al. 2015), which makes a clear compar- ison of the REEs phytoextraction potential of different plant The development of new technologies that use REEs is the main species impossible. Even the comparison of BCF values is not cause of their transport to the environment. Currently, our enough as regards the high amount of environmental factors that knowledge of the distribution of REEs (especially LREEs and influence REEs phytoextraction in plants, therefore promising HREEs) and their phytoextraction from the soils in the vicinity plants for phytoremediation (e.g., Helianthus annuus)can be of roads is very limited. The results of this paper confirm that the characterized by BCF < 1 (Kötschau et al. 2014). concentration of REEs decreases with distance from the road, The plants studied in this paper are commonly found in the which was the expected conclusion. On the other hand, differ- vicinity of roads. The biomass of these plants is many times ences in REEs phytoextraction among some of the most com- higher than many other plant species growing individually near monly occurring roadside plants underlined their potential to roads. For this reason, phytoextraction of numerous elements decontaminate soils. All three herbaceous plant species are small (including REEs) can be highly effective. Although there is clear with low biomass but they usually grow in dense groups of evidence of the harmful influence of REEs on human health specimens per size area. The most effective, T. repens L., may (Pagano et al. 2015a) and plant development (Zhang et al. be especially useful for phytoextraction purposes but the other 2013), the authors have no access to literature where similar two plant species are, in our opinion, promising and would merit studies can be found. On the other hand, there are some data further investigation. Additionally, it is worth emphasizing that that describe or compare the herbaceous plant species tested in to determine an ecological problem of the presence of REEs in our study. Malinowska et al. (2015) revealed that Taraxacum the environment it is necessary, and sufficient, to conduct an spec. was more effective in Cu and Zn phytoextraction than analysis of Ce, Er, and Nd concentration. Achillea millefolium L., Rumex acetosa L., or Vicia cracca L. Acknowledgements This study is a part of a Ph.D. thesis by Patrycja independently of the distance from the road. Diatta et al. (2003), Mleczek and was supported by the Polish Ministry of Science and who analyzed T. officinale, showed this plant species to be a Higher Education of Poland through statutory funds of the Department bioindicator of soil contamination. Both the high efficiency of of Ecology and Environmental Protection, Poznan University of Life element phytoextraction and negative changes in leaf anatomy Sciences. (changes in morphology) were described by Bini et al. (2012), who found that this species is highly effective in the Open Access This article is distributed under the terms of the Creative phytoextraction of toxic elements, in both roots and stems (high Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, values of translocation factor). A great affinity for effective distribution, and reproduction in any medium, provided you give appro- phytoextraction of many other elements was also described by priate credit to the original author(s) and the source, provide a link to the Bech et al. (2016), who showed that T. officinale can be charac- Creative Commons license, and indicate if changes were made. terized by diverse translocation of As, Pb, and Zn in its plant organs (roots, stem) depending on the mineral composition of soils. Based on these findings, we can assume that this species References would also possess high phytoextraction potential for other ele- ments, such as REEs. This was confirmed in our paper by the Abechi ES, Okunola OJ, Zubairu SMJ, Usman AA, Apene E (2010) higher phytoextraction of REEs observed in this species com- Evaluation of heavy metals in roadside soils of major streets in Jos pared to A. vulgaris. Durães et al. (2014)did notfindany cor- metropolis. Nigeria J Environ Chem Ecotoxicol 2:98–102 Adedeji OH, Olayinka OO, Oyebanji FF (2013) Assessment of traffic relation between the concentration of REEs in the rhizosphere related heavy metals pollution of roadside soils in emerging urban and in plants, which suggests that transport of REEs from the centres in Ijebu-north area of Ogun State, Nigeria. J Appl Sci environment to the plant can occur in other ways. 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Environmental Science and Pollution Research – Springer Journals
Published: Jun 5, 2018
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